The DOI matches its Crossref record; 65 of the 66 references it cites were found in a registry or an index; none of the 44 sources its claims cite is checked for support yet.
The frequency of influenza and bacterial coinfection: a systematic review and meta-analysis.
Open accessAbstract
Aim: Coinfecting bacterial pathogens are a major cause of morbidity and mortality in influenza. However, there remains a paucity of literature on the magnitude of coinfection in influenza patients. Method: A systematic search of Me SH , Cochrane Library, Web of Science, SCOPUS , EMBASE , and PubMed was performed. Studies of humans in which all individuals had laboratory confirmed influenza, and all individuals were tested for an array of common bacterial species, met inclusion criteria. Results: Twenty‐seven studies including 3215 participants met all inclusion criteria. Common etiologies were defined from a subset of eight articles. There was high heterogeneity in the results ( I 2 = 95%), with reported coinfection rates ranging from 2% to 65%. Although only a subset of papers were responsible for observed heterogeneity, subanalyses and meta‐regression analysis found no study characteristic that was significantly associated with coinfection. The most common coinfecting species were Streptococcus pneumoniae and Staphylococcus aureus , which accounted for 35% (95% CI , 14%–56%) and 28% (95% CI , 16%–40%) of infections, respectively; a wide range of other pathogens caused the remaining infections. An assessment of bias suggested that lack of small‐study publications may have biased the results. Conclusions: The frequency of coinfection in the published studies included in this review suggests that although providers should consider possible bacterial coinfection in all patients hospitalized with influenza, they should not assume all patients are coinfected and be sure to properly treat underlying viral processes. Further, high heterogeneity suggests additional large‐scale studies are needed to better understand the etiology of influenza bacterial coinfection.
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TL;DR
This systematic review and meta-analysis found that bacterial coinfection in laboratory-confirmed influenza patients was highly variable across studies, with reported rates from 2% to 65%. Streptococcus pneumoniae and Staphylococcus aureus were the most common coinfecting pathogens, but heterogeneity was too high to support a single pooled coinfection estimate.
Key findings
- Twenty-seven studies including 3215 participants met inclusion criteria; reported bacterial coinfection ranged from 2% to 65%, with high heterogeneity (I² = 95%).
- Among eight studies with species-level data (334 patients), S. pneumoniae accounted for 35% (95% CI, 14%–56%) and S. aureus for 28% (95% CI, 16%–40%) of identified coinfecting bacteria.
- After excluding seven studies that contributed more than 50% of heterogeneity, the remaining 20 studies representing 64% of patients had coinfection proportions between 11% and 35% (I² = 37%).
- No study characteristic examined—age, setting, enrollment year, study design, study size, or bacterial collection/detection method—was significantly associated with coinfection frequency.
Methods
- Systematic review and meta-analysis reported per PRISMA, searching MeSH, Cochrane Library, Web of Science, SCOPUS, EMBASE, and PubMed in August 2014; inclusion required human studies with all individuals having laboratory-confirmed influenza and all tested for common bacterial species.
- Data from 27 observational studies (13 prospective, 14 retrospective) were extracted; most enrolled hospitalized patients, with 11 studies focused on ICU patients, 10 on non-ICU hospitalized patients, 3 on ED patients, and 2 on mixed inpatient/outpatient settings.
- Coinfection frequency was analyzed using the DerSimonian-Laird method in R’s metafor package; heterogeneity was quantified with I², and meta-regression, leave-one-out analysis, and Cook’s distances were used to explore heterogeneity.
Limitations
- The paper states that the sample of 27 studies and >3000 patients is small relative to annual influenza-related hospitalizations; studies included only hospitalized patients with moderate to severe influenza, so outpatients and asymptomatic patients are not represented.
- The paper states that bacterial detection methods varied in sensitivity and sampling site, potentially underdiagnosing difficult-to-detect bacteria; antibiotic use before or at enrollment was not systematically assessed and may have led to underestimation.
- The paper states that significant heterogeneity could not be explained by measured study characteristics; evident from the text, all included studies were observational and most were small cohort studies, with selection bias and data-collection reliability concerns noted in the quality assessment.
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A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“A total of 27 articles encompassing 3215 patients met all the inclusion criteria and were included in the final analysis.28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53, 54”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Study screening and selection
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- The authors state this as an assumption: Coinfection was assumed to be any acute bacterial infection identified in respiratory secretions, sputum, or sterile site (e.g., bacteremia).
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“All 27 included studies were observational, of which 13 (1218 patients) were prospective studies,30, 32, 33, 36, 40, 41, 43, 44, 48, 49, 50, 51, 52 and 14 (1997 patients) were retrospective analyses (Table 1).”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Study characteristics
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In the paper
“Using Cook's distances to identify studies that most greatly affected the heterogeneity and results, we found that seven studies contributed more than 50% of the heterogeneity.29, 31, 34, 39, 40, 45, 46”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Bacterial coinfection
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In the paper
“While studies were generally representative of the targeted population, most studies did not report the percentage of patients that agreed to participate.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Assessment of bias
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Among the individual studies, the proportion of bacterial coinfection ranged from 2% (newborns born in USA) to 65% (immunocompetent adults in France) (Figure 3).”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Bacterial coinfection
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passes- The authors state this as an assumption: Coinfection was assumed to be any acute bacterial infection identified in respiratory secretions, sputum, or sterile site (e.g., bacteremia).
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Egger's test of asymmetry was also significant for bias (P = 0·0004).”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Assessment of bias
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The median sample size was 51 (IQR, 18·5–101), and the mean was 119 (SD: 203), which was driven by three large studies29, 44, 53 that contributed 1958 (61%) of the total number of patients included in this analysis.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Study characteristics
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Of those 27, only eight studies, with 334 patients, provided the numbers or percentages of each bacterial coinfecting pathogen.28, 32, 33, 34, 38, 43, 46, 47”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Study screening and selection
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- The authors state this as an assumption: Coinfection was assumed to be any acute bacterial infection identified in respiratory secretions, sputum, or sterile site (e.g., bacteremia).
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Severity of illness varied among studies, but all were focused on hospitalized patients, suggesting a greater than average severity.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Study characteristics
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“High statistical heterogeneity of the included studies (I 2 = 95%) removed confidence in reporting an estimate of the pooled mean proportion of bacterial coinfection through meta‐analysis.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Bacterial coinfection
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- The authors state this as an assumption: Coinfection was assumed to be any acute bacterial infection identified in respiratory secretions, sputum, or sterile site (e.g., bacteremia).
- Probably not a substantial claim. 20
- It may state two separate claims as one. 33
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The majority (21) of studies were cohort studies, and the rest were case–control studies.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Study characteristics
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
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In the paper
“The average quality of the studies was moderate, with the most common quality issues being related to study design, selection biases, and data collection (Table S2).”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Assessment of bias
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
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In the paper
“Most studies enrolled only adults, although the lower age cutoffs varied (e.g., some studies considered adults older than 14 while others used 21).”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Study characteristics
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
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In the paper
“Only seven studies (1214 patients) focused on young children or newborns,29, 31, 38, 46, 49, 51, 54 and two studies (504 patients) included both children and adults.42, 53”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Study characteristics
Strength:plain· not yet calibratedn = 1,214Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
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In the paper
“A funnel plot appeared asymmetrical (Figure 2), suggesting statistical heterogeneity; in particular, there seems to have been a lack of smaller studies with lower rates of bacterial coinfection.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Assessment of bias
Strength:hedged· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The median sample size was 51 (IQR, 18·5–101), and the mean was 119 (SD: 203), which was driven by three large studies29, 44, 53 that contributed 1958 (61%) of the total number of patients included in this analysis.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Study characteristics
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“All 27 included studies were observational, of which 13 (1218 patients) were prospective studies,30, 32, 33, 36, 40, 41, 43, 44, 48, 49, 50, 51, 52 and 14 (1997 patients) were retrospective analyses (Table 1).”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Study characteristics
Strength:plain· not yet calibratedn = 1,218Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
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In the paper
“Fifteen of the studies (1885 patients) began enrollment in 2009 or later,28, 32, 33, 34, 35, 37, 39, 41, 42, 44, 46, 48, 49, 53, 54 and of these, all but one was specifically focused on the 2009 H1N1 pandemic strain.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Study characteristics
Strength:plain· not yet calibratedn = 1,885Tests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“However, results from the bias assessment suggest that the largest potential source of bias was the fact that all the studies were observational studies, and most were small cohort studies.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Assessment of bias
Strength:hedged· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Patients enrolled in the ICU had a slightly higher frequency of coinfection than patients enrolled elsewhere, although this was also not statistically significant (P = 0·14).”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Bacterial coinfection
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In the paper
“Finally, study design (P = 0·47) and bacterial coinfection collection and detection methods (each was tested independently and all P‐values were greater than 0·05) were also not significant.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Bacterial coinfection
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In the paper
“In addition, other Staphylococcal pathogens such as S. epidermidis, and Gram‐negative bacteria, such as Escherichia coli and Moraxella catarrhalis, were also frequently found.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Species‐level analysis
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In the paper
“Although heterogeneity was greater in the pediatric studies (I 2 = 98%) than in the adult studies (I 2 = 89%), coinfection frequency was statistically the same (P = 0·47).”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Bacterial coinfection
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None of the sources cited for this claim have been checked yet.
In the paper
“Only four studies explicitly measured and reported on comorbidities of patients with coinfection and found that older age,28, 44, 53 a higher APACHE II (Acute Physiology and Chronic Health Evaluation II) score,44, 53 diabetes,33 and sepsis33 were risk factors for coinfection.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Bacterial coinfection
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In the paper
“Further, some studies only included severely immunocompromised patients who had concurrent malignancy or organ transplant,31, 33, 49 while others excluded immunocompromised patients.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Bacterial coinfection
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In the paper
“Only three studies excluded participants based on antibiotic use and reported coinfection rates of 12·2%, 26·7%, and 46·6%.28, 34, 36”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Bacterial coinfection
What the sources say
- Not checked yetcites [28] Ahn S, Kim WY, Kim SH et al Role of procalcitonin and C‐reactive protein in differentiation of mixed bacterial infection from 2009 H1N1 viral pneumonia. Influenza Other Respi Viruses 2011; 5: 398– 403. PMC5780656 21668682 source
- Not checked yetcites [34] Cuquemelle E, Soulis F, Villers D et al Can procalcitonin help identify associated bacterial infection in patients with severe influenza pneumonia? A multicentre study. Intensive Care Med 2011; 37: 796– 800. 21369807 PMC7080069 source
- Not checked yetcites [36] Falsey AR, Becker KL, Swinburne AJ et al Bacterial complications of respiratory tract viral illness: a comprehensive evaluation. J Infect Dis 2013; 208: 432– 441. 23661797 PMC3699009 source
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In the paper
“The predominant coinfecting organism in the studies was S. pneumoniae followed by S. aureus, but many other organisms were also found to cause infections.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Conclusion
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In the paper
“Consistent with the prior literature,55, 62 we found that S. pneumoniae was the most frequent bacterial coinfection; however, both S. aureus and other bacterial coinfections were also quite common.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Discussion
What the sources say
- Not checked yetcites [55] Brundage JF. Interactions between influenza and bacterial respiratory pathogens: implications for pandemic preparedness. Lancet Infect Dis 2006; 6: 303– 312. 16631551 PMC7106411 source
- Not checked yetcites [62] McCullers JA. The co‐pathogenesis of influenza viruses with bacteria in the lung. Nat Rev Micro 2014; 12: 252– 262. 24590244 source
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In the paper
“We found that bacterial coinfection of hospitalized patients with influenza is often common, although results were highly heterogeneous.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Conclusion
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In the paper
“Lung tissue samples from the 1918 influenza pandemic suggest that the majority of the estimated 20–60 million deaths were from bacterial infections rather than from direct effects of the virus.3”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Introduction
What the sources say
- Not checked yetcites [3] Morens DM, Taubenberger JK, Fauci AS. Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J Infect Dis 2008; 198: 962– 970. 18710327 PMC2599911 source
Strength:hedged· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“The potential bias of each study was assessed using the Quality Assessment Tool for Quantitative Studies developed by the National Collaborating Centre for Methods and Tools.20”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Methods > Assessment of bias
What the sources say
- Not checked yetcites [20] National Collaborating Centre for Methods and Tools. Quality Assessment Tool for Quantitative Studies. Vol (Updated 13 April. Hamilton. ON: McMaster University, 2010; 2008.
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
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In the paper
“Sources of data were carefully reviewed by BM, AG, EK, and studies reporting already included data were excluded (the study with the earlier publication date was considered the primary study, and all others excluded).”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Methods > Data extraction
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In the paper
“The full text of all studies meeting the criteria and those for which a conclusion could not be made were reviewed independently by the two authors. Disagreements were resolved through consultation with a third party.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Methods > Selection of studies
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None of the sources cited for this claim have been checked yet.
In the paper
“In seasonal epidemics, influenza bacterial coinfection is associated with increases in hospital admissions,4, 5 more severe symptoms,6 and increases in mortality.7”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Introduction
What the sources say
- Not checked yetcites [4] Masiá M, Padilla S, Antequera P, Ramos JM, Ruiz M, Gutiérrez F. Predictors of pneumococcal co‐infection for patients with pandemic (H1N1) 2009. Emerg Infect Dis 2011; 17: 1475. 21801627 PMC3381536
- Not checked yetcites [5] Blyth CC, Webb SA, Kok J et al The impact of bacterial and viral co‐infection in severe influenza. Influenza Other Respir Viruses 2013; 7: 168– 176. 22487223 PMC5006004 source
- Not checked yetcites [6] Cillóniz C, Ewig S, Menéndez R et al Bacterial co‐infection with H1N1 infection in patients admitted with community acquired pneumonia. J Infect 2012; 65: 223– 230. 22543245 PMC7132402 source
- Not checked yetcites [7] Paddock CD, Liu L, Denison AM et al Myocardial injury and bacterial pneumonia contribute to the pathogenesis of fatal influenza B virus infection. J Infect Dis 2012; 205: 895– 905. 22291193 source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
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In the paper
“Two authors (BM, AG) extracted study data from all included publications independently, and results were then compared. Differences were resolved by consensus.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Methods > Data extraction
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Two authors (BM, AG) independently screened the title and abstract of all the search‐returned publications to determine whether they met study criteria.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Methods > Selection of studies
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“We conducted a systematic review, which is reported in accordance with PRISMA guidelines,19 to determine the frequency of bacterial coinfection among individuals with laboratory confirmed influenza.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Methods
What the sources say
- Not checked yetcites [19] Liberati A, Altman DG, Tetzlaff J et al The PRISMA statement for reporting systematic reviews and meta‐analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 2009; 339:b2700. doi: 10.1136/bmj.b2700. PMC2714672 19622552 source
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What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Inclusion was restricted to studies of humans in which all individuals had laboratory confirmed influenza, and all individuals were tested for an array of common bacterial species.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Methods
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim. It may state two separate claims as one.
In the paper
“Identification of coinfected patients and coinfecting pathogen enables clinicians to initiate appropriate antibiotic therapy and improve patient outcomes.12”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Introduction
What the sources say
- Not checked yetcites [12] Van‐Tam J, Sellwood C. Pandemic Influenza. Boston: CABI, 2012. source
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In the paper
“Funnel plots and calculation of Egger's test of asymmetry were also used to assess biases such as publication and small‐study effects.23”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Methods > Assessment of bias
What the sources say
- Not checked yetcites [23] Egger M, Smith GD, Schneider M, Minder C. Bias in meta‐analysis detected by a simple, graphical test. BMJ 1997; 315: 629– 34. 9310563 PMC2127453 source
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In the paper
“Studies were also not fully clear on the reliability of the tools used for data collection, which made it difficult to eliminate this as a potential source of bias in the strains detected.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Assessment of bias
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In the paper
“This tool was selected for its comprehensive ability to assess the methodological quality of non‐randomized studies and has shown good reliability and validity.21, 22”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Methods > Assessment of bias
What the sources say
- Not checked yetcites [21] Thomas BH, Ciliska D, Dobbins M, Micucci S. A process for systematically reviewing the literature: providing the research evidence for public health nursing interventions. Worldviews Evid Based Nurs 2004; 1: 176– 184. 179p. 17163895 source
- Not checked yetcites [22] Deeks J, Dinnes J, D'Amico R, Sowden A, Sakarovitch C. Evaluating non‐randomised intervention studies. Health Technol Assess 2003; 7: 186. 14499048 source
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Each study was independently evaluated by two authors, and discrepancies regarding bias assessment were resolved by consensus.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Methods > Assessment of bias
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“However, there was some suggestion that negative findings or low levels of bacterial coinfection were not published.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Discussion
Strength:hedged· not yet calibratedCausal:conditional· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Antibiotic use at the time of, or prior to enrollment, was another factor that may have contributed to significant heterogeneity, but could not be systematically assessed.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Bacterial coinfection
Strength:hedged· not yet calibratedCausal:conditional· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
In the paper
“This diverse profile of coinfecting pathogens confirms current Infectious Disease Society of America (IDSA) recommendations for broad‐spectrum antibiotic coverage for influenza‐related pneumonia.63”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Discussion
What the sources say
- Not checked yetcites [63] Harper SA, Bradley JS, Englund JA et al Seasonal influenza in adults and children—diagnosis, treatment, chemoprophylaxis, and institutional outbreak management: clinical practice guidelines of the Infectious Diseases Society of America. Clin Infect Dis 2009; 48: 1003– 1032. 19281331 PMC7107965 source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim.
In the paper
“Given that over 25% of identified isolates were S. aureus, and that approximately 50% of hospital S. aureus isolates are MRSA,64 our study supports IDSA recommendations for empiric coverage of CA‐MRSA in influenza‐related pneumonia patients.63”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Discussion
What the sources say
- Not checked yetcites [63] Harper SA, Bradley JS, Englund JA et al Seasonal influenza in adults and children—diagnosis, treatment, chemoprophylaxis, and institutional outbreak management: clinical practice guidelines of the Infectious Diseases Society of America. Clin Infect Dis 2009; 48: 1003– 1032. 19281331 PMC7107965 source
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Our findings suggest that while patients hospitalized with moderate to severe influenza may be coinfected with both viral and bacterial pathogens, many patients will likely not be coinfected.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Discussion
Load-bearingStrength:hedged· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“This lack of statistically significant variability may be due to unrecorded differences in the studies, such as genetic differences in the populations, local differences in either the severity of viral or bacterial illness, unrecorded patient comorbidities, variation in treatment, or as noted above, antibiotic use (either current or past).”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Discussion
Strength:hedged· not yet calibratedCausal:conditional· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Second, studies included only patients who were hospitalized for influenza and thus represent a population with moderate to severe influenza.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Discussion
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Although a few studies enrolled patients in the outpatient or ED setting, all required hospitalization.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Discussion
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Hence, these results may underrepresent the actual number of bacterial coinfections and the distribution of the pathogens of those coinfections.”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Discussion
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
In the paper
“One study found that previous antibiotic use made patients more likely to acquire atypical bacterial infections.50”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Bacterial coinfection
What the sources say
- Not checked yetcites [50] Van Gageldonk‐Lafeber AB, Wever PC, Van DL et al The aetiology of community‐acquired pneumonia and implications for patient management. Neth J Med 2013; 71: 418– 425. 24127502
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“For example, Bjarnason and colleagues found that none of the patients using antibiotics were in the coinfected group and when they excluded antibiotic users from the study, the prevalence of coinfection increased from 14% to 45%.30”
§ The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis > Results > Bacterial coinfection
What the sources say
- Not checked yetcites [30] Bjarnason A, Thorleifsdottir G, Love A et al Severity of influenza A 2009 (H1N1) pneumonia is underestimated by routine prediction rules. Results from a prospective, population‐based study. PLoS ONE 2012; 7: e46816. 23071646 PMC3469650 source
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
The authors state this as an assumption.
Coinfection was assumed to be any acute bacterial infection identified in respiratory secretions, sputum, or sterile site (e.g., bacteremia).
“Coinfection was assumed to be any acute bacterial infection identified in respiratory secretions, sputum, or sterile site (e.g., bacteremia).”
The paper relies on this without support.
Differentiating viral from bacterial infection remains a challenge for clinicians.
“Differentiating viral from bacterial infection remains a challenge for clinicians.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“The frequency of influenza and bacterial co-infection ranged from 2% to 65%.”
From Oral Microbiome and SARS-CoV-2: Beware of Lung Co-infection (2020) · cites this paper as Klein et al., 2016
In the citing paper
“Among them, Streptococcus pneumoniae and Staphylococcus aureus, which accounted for 35% and 28% of infections (Klein et al., 2016).”
From Oral Microbiome and SARS-CoV-2: Beware of Lung Co-infection (2020) · cites this paper as Klein et al., 2016
In the citing paper
“The bacteria most commonly associated with influenza infection have been reported to be those which commonly colonise the nasopharynx, such as Streptococcus pneumoniae, Staphylococcus aureus, and Streptococcus pyogenes, with secondary infection usually occurring in the first 6 days of influenza.43, 44, 45”
From Co-infections in people with COVID-19: a systematic review and meta-analysis. (2020) · cites this paper as [45]
In the citing paper
“Studies have shown that up to 65% of laboratory confirmed cases of influenza infection exhibited bacterial co/secondary infection, although Klein et al. (2016) state that in the majority of the research included in their meta-analysis this figure ranged between 11 and 35%.”
From Secondary bacterial infections associated with influenza pandemics (2017) · cites this paper as Klein et al., 2016
In the citing paper
“M. catarrhalis has been highlighted as a frequent source of co-infection for influenza since the early 1980’s (Klein et al., 2016).”
From Secondary bacterial infections associated with influenza pandemics (2017) · cites this paper as Klein et al., 2016
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Mixed-setting total includes an uncounted third study
MinorThe two cited mixed-setting studies have 833 and 160 patients, totaling 993 rather than 1100. Table 1 lists a third mixed-setting study, Carr et al. (107 patients), which brings the total to 1100.
Reported 1100 · recomputed 993
“2 enrolled patients in a mix of inpatient and outpatient settings (1100 patients).29, 52”
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Metadata
- Authors
- Klein, E. Y., Monteforte, B., Gupta, A., Jiang, W., May, L., Hsieh, Y., & Dugas, A.
- Affiliations
- Center for Disease Dynamics, Economics & Policy (US)
- Eastern Virginia Medical School (US)
- Allegheny General Hospital (US)
- George Washington University (US)
- Johns Hopkins University (US)
- Corresponding author
- Klein, Eili Y.
- Venue
- Influenza and Other Respiratory Viruses
- Publisher
- Wiley
- Published
- 2016-06-24
- Volume
- 10
- Issue
- 5
- Pages
- 394-403
- ISSN
- 1750-2640 (ISSN-L)
- 1750-2659
- PMC
- PMC4947938
- OpenAlex
- W2402456610
- Semantic Scholar
- 210ca1b97c01c947b269aac6fab9f37485337e22
- Cited by
- 574
- References
- 66
- Citations by year
- 2026: 29 · 2025: 46 · 2024: 51 · 2023: 96 · 2022: 104 · 2021: 112 · 2020: 58 · 2019: 20 · 2018: 24 · 2017: 15 · 2016: 5
- FWCI
- 2.89
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Influenza and Other Respiratory Viruses (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Funders
- U.S. Department of Health and Human Services (IDSEP130014‐01‐00)
- Topics
- Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
- Health Sciences › Medicine › Epidemiology › Pneumonia and Respiratory Infections
- Health Sciences › Medicine › Epidemiology › Respiratory viral infections research
- Keywords
- influenza, bacterial co-infection, Streptococcus pneumoniae, Staphylococcus aureus, hospitalized influenza patients, pathogenic bacteria
- MeSH terms
- Adolescent, Adult, Child, Child, Preschool, Female, Hospitalization, Humans, Infant, Infant, Newborn, Influenza, Human, Male, Middle Aged, Pneumococcal Infections, Staphylococcal Infections, Streptococcus pneumoniae, Drug Resistance, Bacterial, Methicillin-Resistant Staphylococcus aureus, Young Adult, Coinfection
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
A language model drew the claims from the paper on 2026-10-09, under version 3 of the claim definition (model deepseek-v4.1-flash, prompt extract-v3).
A second model labelled each claim on 2026-10-09 (model jev-1.13-20260917, definition revision gold-guideline-v0.2).
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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